Cognition, 50 (1994) 7-15

OOlO-0277/94/$07.00 0 1994 - Elsevier Science B.V. All rights reserved.

Insensitivity to future consequences

following damage to human prefrontal
cortex

Antoine Bechara, Antonio R. Damasio*, Hanna Damasio,

Steven W. Anderson
Department of Neurology, Division of Behavioral Neurology and Cognitive Neuroscience,
University of Iowa College of Medicine, Iowa City, IA 52242, USA

Abstract

Following damage to the ventromedial prefrontal cortex, humans develop a defect

in real-life decision-making, which contrasts with otherwise normal intellectual
functions. Currently, there is no neuropsychological probe to detect in the
laboratory, and the cognitive and neural mechanisms responsible for this defect
have resisted explanation. Here, using a novel task which simulates real-life
decision-making in the way it factors uncertainty of premises and outcomes, as well
as reward and punishment, we find that prefrontal patients, unlike controls, are
oblivious to the future consequences of their actions, and seem to be guided by
immediate prospects only. This finding offers, for the first time, the possibility of
detecting these patients’ elusive impairment in the laboratory, measuring it, and
investigating its possible causes.

Introduction

Patients with damage to the ventromedial sector of prefrontal cortices develop

a severe impairment in real-life decision-making, in spite of otherwise preserved
intellect. The impairments are especially marked in the personal and social realms
(Damasio, Tranel, & Damasio, 1991). Patient E.V.R. is a prototypical example of
this condition. He often decides against his best interest, and is unable to learn

*Corresponding author.
Supported by NINDS PO1 NS19632 and the James S. McDonnell Foundation.

SSDZ OOlO-0277(93)00606-8
from his mistakes. His decisions repeatedly lead to negative consequences. In
striking contrast to this real-life decision-making impairment, E.V.R.‘s general
intellect and problem-solving abilities in a laboratory setting remain intact. For
instance, he produces perfect scores on the Wisconsin Card Sorting Test (Milner,
1963), his performances in paradigms requiring self-ordering (Petrides & Milner.
1982), cognitive estimations (Shallice & Evans, 1978), and judgements of recency
and frequency (Milner, Petrides, & Smith, 1985) are flawless; he is not presevera-
tive, nor is he impulsive; his knowledge base is intact and so is his short-term and
working memory as tested to date; his solution of verbally posed social problems
and ethical dilemmas is comparable to that of controls (Saver & Damasio, 1991).
The condition has posed a double challenge, since there has been neither a
satisfactory account of its physiopathology, nor a laboratory probe to detect and
measure an impairment that is so obvious in its ecological niche. Here we describe
an experimental neuropsychological task which simulates, in real time, personal
real-life decision-making relative to the way it factors uncertainty of premises and
outcomes, as well as reward and punishment. We show that. unlike controls,
patients with prefrontal damage perform defectively and are seemingly insensitive
to the future.

Materials and methods

The subjects sit in front of four decks of cards equal in appearance and size,
and are given a $2000 loan of play money (a set of facsimile US bills). The
subjects are told that the game requires a long series of card selections, one card
at a time, from any of the four decks. until they are told to stop. After turning
each card, the subjects receive some money (the amount is only announced after
the turning, and varies with the deck). After turning some cards, the subjects are
both given money and asked to pay a penalty (again the amount is only
announced after the card is turned and varies with the deck and the position in
the deck according to a schedule unknown to the subjects). The subjects are told
that (1) the goal of the task is to maximize profit on the loan of play money, (2)
they are free to switch from any deck to another. at any time, and as often as
wished. but (3) they are not told ahead of time how many card selections must be
made (the task is stopped after a series of 100 card selections). The prc-
programmed schedules of reward and punishment are shown on the score cards
(Fig. 1). Turning any card from deck A or deck B yields $100; turning any card
from deck C or deck D yields $50. However, the ultimate future yield of each
deck varies because the penalty amounts arc higher in the high-paying decks (A
and B). and lower in the low-paying decks (C and D). For example, after turning
10 cards from deck A, the subjects have earned $1000, but they have also
encountered 5 unpredicted punishments bringing their total cost to $1250, thus
 A. Bechara et al. I Cognition 50 (1994) 7-15 9

s! SL- 1%
CP OS- 6 a
m OOE- 0 Isz -

a
incurring a net loss of $250. The same happens on deck 9. On the other hand,
after turning 10 cards from decks C or D, the subjects earn $500, but the total of
their unpredicted punishments is only $250 (i.e. subject nets $250). In summary.
decks A and B are equivalent in terms of overall net loss over the trials. The
difference is that in deck A, the punishment is more frequent, but of smaller
magnitude. whereas in deck 9. the punishment is less frequent, but of higher
magnitude. Decks C and D are also equivalent in terms of overall net loss. In
deck C. the punishment is more frequent and of smaller magnitude. while in deck
D the punishment is less frequent but of higher magnitude. Decks A and B are
thus “disadvantageous” because they cost the most in the long run, while decks C
and D are “advantageous” because they result in an overall gain in the long run.
The performances of a group of normal control subjects (21 women and 23
men) in this task were compared to those of E.V.R. and other frontal lobe
subjects (4 men and 2 women). The age range of normal controls was from 20 to
79 years; for E.V.R.-like subjects it was from 43 to 84 years. About half the
number of subjects in each group had a high school education. and the other half
had a college education. E.V.R.-like subjects were retrieved from the Patient
Registry of the Division of Behavioral Neurology and Cognitive Neuroscience.
Selection criteria wet-c the documented presence of abnormal decision-making
and the existence of lesions in the ventromedial prefrontal region.
To determine whether the defective performance of E.V.R.-like subjects on the
task is specific to ventromedial frontal lobe damage, and not merely caused by
brain damage in general. we compared the pcrformanccs of E.V.R.-like subjects
and normal controls, to an education matched group of brain-damaged controls.
There were 3 women and 6 men, rangin, 0 in age from 20 to 71 years. These
controls were retrieved from the same Patient Registry and were chosen so as to
have lesions in occipital. temporal and dorsolatcral frontal regions. Several of the
brain-damaged controls had memory defects. as revealed by conventional neuro-
psychological tests.
Finally. to determine what would happen to the performance if it were
repeated over time, we retested the target subjects and a smaller sample of
normal controls (4 women and I man between the ages of 20 and 55, matched to
E.V.R. in level of education) after various time intervals (one month after the first
test. 24 h later. and for the fourth time. six months later).

Results

Fig. 2 (left) shows that normal controls make more selections from the good
decks (C and D), and avoid the bad decks (A and 9). In sharp contrast.
E.V.R.-like subjects select fewer from the good decks (C and D), and choose
more from the bad decks (A and 9). The differcncc is significant. An analysis of
A. Bechara et al. / Cognition SO (1994) 7-15 11
12 A. Brchara ct al. ! Cognition 50 (1994) 7- 15

variance comparing the number of cards from each deck chosen by normal
controls and by target subjects revealed a significant interaction of group (controls
vs. targets) with choice (A, B, C, D) (F(3,147) = 42.9, p < .OOl). Subsequent
Newman-Keuls r-tests revealed that the number of cards selected by normal
controls from deck A or B were significantly less than the number of cards
selected by target subjects from the same decks (ps < .OOl). On the contrary. the
number of cards selected by controls from decks C or D were significantly higher
than the numbers selected by target subjects (ps < .OOl). Within each group,
comparison of the performances among subjects from different age groups,
gender and education yielded no statistically significant differences.
Fig. 2 (right) shows that a comparison of card selection profiles revealed that
controls initially sampled all decks and repeated selections from the bad decks A
and 9, probably because they pay more, but eventually switched to more and
more selections from the good decks C and D, with only occasional returns to
decks A and B. On the other hand, E.V.R. behaves like normal controls only in
the first few selections. He does begin by sampling all decks and selecting from
decks A and B. and he does make several selections from decks C and D, but
then he returns more frequently and more systematically to decks A and 9. The
other target subjects behave similarly.
Fig. 3 reveals that the performance of brain-damaged controls was no different

v
60-
9
&

“0 1
-40 ’
k7 Normal Brain- Damaged EVR EVR-Type
2
z CONTROLS TARGET SUBJECTS

Fig. 3. Tota! ~zumher oj s&ctions from the udvantugrous decks (C + D) minus the rota/ tzwnhers of.
.srlectioru from the di.sodwnicc~eou~ decks (A + B) from u group of tlormul c~orztrol~s
(II = 34).
brow-dw?ragc~d corwol, (n = 9). E.KR., und E.V.R.-like .subjectY (II = 6). Bars represent
means _C6. e. m. Pfxrtr ve ,suwcs reJect advuntapwo c0ur.w of a&m, und negutivr .scores
 A. Bechara et al. I Cognition 50 (1994) 7-15 13

from that of normal controls, and quite the opposite of the performance of the
prefrontal subjects. One-way ANOVA on the difference in the total numbers of
card selections from the advantageous decks minus the total numbers of selections
from the disadvantageous decks obtained from normal and brain-damaged
controls did not reveal a significant difference between the two groups (F(1,52) =
0.1, p > .l), but the difference between the normal and E.V.R.-like groups was
highly significant (F(1,50) = 74.8, p < .OOl).
As a result of repeated testing, E.V.R.‘s performance did not change, one way
or the other, when tested one month after the first test, 24 h later, and for the
fourth time, six months later. This pattern of impaired performance was also seen
in other target subjects. On the contrary, the performance of normal controls
improved over time.

Discussion

These results demonstrate that E.V.R. and comparable subjects perform

defectively in this task, and that the defect is stable over time. Although the task
involves a long series of gains and losses, it is not possible for subjects to perform
an exact calculation of the net gains or losses generated from each deck as they
play. Indeed, a group of normal control subjects with superior memory and IQ,
whom we asked to think aloud while performing the task, and keep track of the
magnitudes and frequencies of the various punishments, could not provide
calculated figures of the net gains or losses from each deck. The subjects must rely
on their ability to develop an estimate of which decks are risky and which are
profitable in the long run. Thus, the patients’ performance profile is comparable
to their real-life inability to decide advantageously, especially in personal and
social matters, a domain for which in life, as in the task, an exact calculation of
the future outcomes is not possible and choices must be based on approximations.
We believe this task offers, for the first time, the possibility of detecting these
patients’ elusive impairment in the laboratory, measuring it, and investigating its
possible causes.
Why do E.V.R.-like subjects make choices that have high immediate reward,
but severe delayed punishment? We considered three possibilities: (1) E.V.R.-like
subjects are so sensitive to reward that the prospect of future (delayed) punish-
ment is outweighed by that of immediate gain; (2) these subjects are insensitive to
punishment, and thus the prospect of reward always prevails, even if they are not
abnormally sensitive to reward; (3) these subjects are generally insensitive to
future consequences, positive or negative, and thus their behavior is always guided
by immediate prospects, whatever they may be. To decide on the merit of these
possibilities, we developed a variant of the basic task, in which the schedules of
reward and punishment were reversed, so that the punishment is immediate and
14 A. Bechara et al. I Cognition SO (1994) 7-15

the reward is delayed. The profiles of target subjects in that task suggest that they
were influenced more by immediate punishment than by delayed reward (un-
published results). This indicates that neither insensitivity to punishment nor
hypersensitivity to reward are appropriate accounts for the defect. A qualitative
aspect of the patients’ performance also supports the idea that immediate
consequences influence the performance significantly. When they are faced with a
significant money loss in a given deck, they refrain from picking cards out of that
same deck, for a while, just like normals do, though unlike normals they then
return to select from that deck after a few additional selections. When we
combine the profiles of both basic task and variant tasks, we are left with one
reasonable possibility: that these subjects are unresponsive to future conse-
quences, whatever they are. and are thus more controlled by immediate
prospects.
How can this “myopia” for the future be explained? Evidence from other
studies suggests that these patients possess and can access the requisite knowledge
to conjure up options of actions and scenarios of future outcomes just as normal
controls do (Saver 6i Damasio, 1991). Their defect seems to be at the level of
acting on such knowledge. There are several plausible accounts to explain such a
defect. For instance, it is possible that the representations of future outcomes that
these patients evoke are unstable, that is, that they are not held in working
memory long enough for attention to enhance them and reasoning strategies to be
applied to them. This account invokes a defect along the lines proposed for
behavioral domains dependent on dorsolateral prefrontal cortex networks, and
which is possibly just as valid in the personal/social domain of decision-making
(Goldman-Rakic, 1987). Defects in temporal integration and attention would fall
under this account (Fuster, 1989; Posner. 1986). Alternatively, the representa-
tions of future outcomes might be stable, but they would not be marked with a
negative or positive value, and thus could not be easily rejected or accepted. This
account invokes the somatic marker hypothesis which posits that the overt or
covert processing of somatic states provides the value mark for a cognitive
scenario (Damasio, 1994; Damasio et al., 1991). We have been attempting to
distinguish between these two accounts in a series of subsequent experiments
using this task along with psychophysiological measurements. Preliminary results
favor the latter account, or a combination of the two accounts. Those results also
suggest that the biasing effect of the value mark operates covertly, at least in the
early stages of the task.

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